The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA

Plant Journal

Volumn 33, Issue 1, 2003, Pages 47-59

  Yang, Yingzhen ^a   Fanning, Laura ^a   Jack, Thomas ^a  

^a Dartmouth College   (United States)

Author keywords

APETALA3; Arabidopsis; Dimerization; K domain; Leucine zipper; MADS; PISTILLATA

Indexed keywords

AMINO ACIDS; DIMERIZATION; DNA; GENES; HYDROPHOBICITY; MUTAGENESIS; PROTEINS;

LEUCINE ZIPPER MOTIFS;

PLANTS (BOTANY);

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DIMERIZATION; FLOWERS; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS;

EID: 0037244198     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.0960-7412.2003.01473.x     Document Type: Review

References (64)

1. Alvarez-Buylla, E.R., Liljegren, S.J., Pelaz, S., Gold, S.J., Burgeff, C., Ditta, G.S., Vergara-Silva, F. and Yanofsky, M.F. (2000a) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cell, roots, and trichomes. Plant J. 24, 1-11.
2. Alvarez-Buylla, E.R., Pelaz, S., Liljegren, S.J., Gold, S.E., Burgeff, C., Ditta, G.S., de Pouplana, L.R., Martinez-Castilla, L. and Yanofsky, M.F. (2000b) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl Acad. Sci. USA, 97, 5328-5333.
3. Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Meth Mol. Biol. 82, 259-266.
4. Becker, A., Kaufmann, K., Freialdenhoven, A., Vincent, C., Li, M.-A., Saedler, H. and Theißen, G. (2002) A novel MADS-box gene subfamily with a sister group relationship to class B floral homeotic genes. Mol. Genet. Genomics, 266, 942-950.
5. Bella, J. and Berman, H.M. (1996) Crystallographic evidence for Cα-⋯H=C hydrogen bonds in a collagen triple helix. J. Mol. Biol. 264, 734-742.
6. Bowman, J.L., Smyth, D.R. and Meyerowitz, E.M. (1989) Genes directing flower development in Arabidopsis. Plant Cell, 1, 37-52.
7. Causier, B., Kieffer, M. and Davies, B. (2002) MADS-box genes reach maturity. Science, 296, 275-276.
8. Cho, S., Jang, S., Chae, S., Chung, K.M., Moon, Y.H., An, G. and Jang, S.K. (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol. Biol. 40, 419-429.
9. Davies, B., Egea-Cortines, M., de Andrade Silva, E., Saedler, H. and Sommer, H. (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 16, 4330-4343.
10. Egea-Cortines, M., Saedler, H. and Sommer, H. (1999) Ternary complex formation between the MADS-box proteins SQUA-MOSA, DEFIClENS, and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 18, 5370-5379.
11. Fan, H.-Y., Hu, Y., Tudor, M. and Ma, H. (1997) Specific interactions between K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant J. 12, 999-1010.
12. Fromant, M., Blanquet, S. and Plateau, P. (1995) Direct random mutagenesis of gene-sized DNA fragments using polymerase chain reaction. Anal. Biochem. 224, 347-353.
13. Glover, J.N.M. and Harrison, S.C. (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature, 373, 257-261.
14. Gonzalez, L., Woolfson, D.N. and Alber, T. (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper. Nature Struct. Biol. 3, 1011-1018.
15. Goto, K. and Meyerowitz, E.M. (1994) Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548-1560.
16. Harbury, P.B., Zhang, T., Kim, P.S. and Alber, T. (1993) A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science, 262, 1401-1407.
17. Hassler, M. and Richmond, T.J. (2001) The B-box dominates SAP-1-SRF interactions in the structure of the ternary complex. EMBO J. 20, 3018-3028.
18. Honma, T. and Goto, K. (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409, 525-529.
19. Horton, R.M. and Pease, L.R. (1991) Recombination and mutagenesis of DNA sequences using PCR. In Directed Mutagenesis, (M.J. McPherson ed.). New York, USA: Oxford University Press, IRL Press, pp. 217-247.
20. Huang, H., Mizukami, Y. and Ma, H. (1993) Isolation and characterization of the binding sequence for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucl Acids Res. 21, 4769-4776.
21. Huang, H., Tudor, M., Su, T., Zhang, Y., Hu, Y. and Ma, H. (1996) DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. Plant Cell, 8, 81-94.
22. Initiative, Arabidopsis Genome (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
23. Jack, T, (2001) Plant development going MADS. Plant Mol. Biol. 46, 515-520.
24. Jack, T., Brockman, L.L. and Meyerowitz, E.M. (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell, 68, 683-697.
25. Jack, T., Fox, G.L. and Meyerowitz, E.M. (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and post-transcriptional regulation determine floral organ identity. Cell, 76, 703-716.
26. James, P., Halladay, J. and Craig, E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
27. Junius, F.K., Mackay, J.P., Bubb, W.A., Jensen, S.A., Weiss, A.S. and King, G.F. (1995) Nuclear magnetic resonance characterization of the Jun leucine zipper domain: unusual properties of coiled-coil interfacial polar residues. Biochemistry, 34, 6164-6174.
28. Kieffer, M. and Davies, B. (2001) Developmental programmes in floral organ formation. Seminars Cell Dev. Biol. 12, 373-380.
29. Kramer, E.M. (2000) Evolution of Genetic Mechanisms Controlling Petal and Stamen Development. PhD Thesis, Yale University, New Haven, Connecticut.
30. Kramer, E.M., Dorit, R.L. and Irish, V.F. (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics, 149, 765-783.
31. Krizek, B.A. and Meyerowitz, E.M. (1996a) The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development, 112, 11-22.
32. Krizek, B.A. and Meyerowitz, E.M. (1996b) Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc. Natl Acad. Sci. USA, 93, 4063-4070.
33. Landschulz, W.H., Johnson, P.F. and McKnight, S.L. (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science, 240, 1759-1764.
34. Li, B. and Fields, S. (1993) Identification of mutations in p53 that affect its binding to SV40 large T antigen by using the yeast two-hybrid system. FASEB J. 7, 957-963.
35. Lumb, K.J. and Kim, P.S. (1995) A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry, 34, 8642-8648.
36. Ma, H., Yanofsky, M.F. and Meyerowitz, E.M. (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495.
37. Mizukami, Y., Huang, H., Tudor, M., Hu, Y. and Ma, H. (1996) Functional domains of the floral regulator AGAMOUS: characterization of the DNA binding domain and analysis of dominant-negative mutations. Plant Cell, 8, 831-845.
38. Moon, Y.-H., Jung, J.-Y., Kang, H.-G. and An, G. (1999) Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol. Biol. 40, 167-177.
39. O'Shea, E.K., Klemm, J.D., Kim, P.S. and Alber, T. (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science, 254, 539-544.
40. O'Shea, E.K., Rutkowski, R. and Kim, P.S. (1992) Mechanism of specificity in Fos-Jun oncoprotein heterodimer. Cell, 68, 699-708.
41. Pellegrini, L., Tan, S. and Richmond, T.J. (1995) Structure of serum response factor core bound to DNA. Nature, 376, 490-498.
42. Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L. and Riechmann, J.L. (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126, 122-132.
43. Reynolds, A., Lundblad, V., Dorris, D. and Keaveney, M. (1998) Yeast vectors and assays for expression of cloned genes. In Current Protocols in Molecular Biology, Vol. 2 (Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl K., eds). New York: John Wiley & Sons, 13.6.1-13.6.6.
44. Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C.-Z., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
45. Riechmann, J.L., Krizek, B.A. and Meyerowitz, E.M. (1996a) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl Acad. Sci. USA, 93, 4793-4798.
46. Riechmann, J.L. and Meyerowitz, E.M. (1997a) Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol. Biol. Cell, 8, 1243-1259.
47. Riechmann, J.L. and Meyerowitz, E.M. (1997b) MADS domain proteins in plant development. Biol. Chem. 378, 1079-1101.
48. Riechmann, J.L., Wang, M. and Meyerowitz, E.M. (1996b) DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucl Acids Res. 24, 3134-3141.
49. Santelli, E. and Richmond, T.J. (2000) Crystal structure of MEF2A core bound to DNA at 1.5 A resolution. J. Mol. Biol. 297, 437-449.
50. Scortecci, K.C., Micheals, S.D. and Amasino, R.M. (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 26, 229-236.
51. Senes, A., Ubarretxena-Belandia, I. and Engelman, D.M. (2001) The Cα-H⋯O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions. Proc. Natl Acad. Sci. USA, 98, 9056-9061.
52. Sieburth, L.E., Running, M.P. and Meyerowitz, E.M. (1995) Genetic separation of third and fourth whorl functions of AGAMOUS. Plant Cell, 7, 1249-1258.
53. Tan, S. and Richmond, T. (1998) Crystal structure of the yeast MATα2/MCM1/DNA ternary complex. Nature, 391, 660-666.
54. Theißen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T.M., nster, T., Winter, K.-U. and Saedler, H. (2000) A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115-149.
55. Theißen, G., Kim, J. and Saedler, H. (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43, 484-516.
56. Tilly, J., Allen, D.W. and Jack, T. (1998) The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APE-TALA3 mediate diverse regulatory effects. Development, 125, 1647-1657.
57. Vidal, M. (1997) The reverse two-hybrid system. In The Yeast Two-Hybrid System (Bartel P.L. and Fields S., eds). New York: Oxford University Press, pp. 109-147.
58. Vinson, C.R., Hai, T. and Boyd, S.M. (1993) Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Genes Dev. 7, 1047-1058.
59. White, M.A. (1996) The yeast two-hybrid system: forward and reverse. Proc. Natl Acad. Sci. USA, 93, 10001-10003.
60. Winter, K.-U., Weiser, C., Kaufmann, K., Bohne, A., Kirchner, C., Kanno, A., Saedler, H. and Theißen, G. (2002) Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization. Mol. Biol. Evol. 19, 587-596.
61. Yang, Y., Xiang, H.M. and Jack, T. (2003) pistillata-S, an Arabidopsis B class mutant with strong defects in petal but not in stamen development. Plannt J. 33, 177-188.
62. Yukenberg, P.D., Witney, F., Geisselsoder, J. and McClary, J. (1991) Site-directed in vitro mutagenesis using uracil-containing DNA and phagemid vectors. In Directed Mutagenesis (McPherson M.J., ed.). New York, USA: Oxford IRL Press, 27-48.
63. Zachgo, S., de Andrade Silva, E., Motte, P., Tröbner, W., Saedler, H. and Schwarz-Sommer, Z. (1995) Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development, 121, 2861-2875.
64. Zeng, X., Herndon, A.M, and Hu, J.C. (1997) Buried asparagines determine the dimerization specificities of leucine zipper mutants. Proc. Natl Acad. Sci. USA, 94, 3673-3678.